塑料已经成为人们日常生活必不可少的部分[1],同时塑料造成的污染已演变成全球环境问题[2]。据估计,全球每年有4.8~12.7百万t的废塑料排放到海洋中[3],对海洋环境及海洋中的生物造成了负面影响。近几年也开始关注塑料在土壤系统中的作用,德国科学家Rillig[4]首次提出微塑料在土壤中累积到一定程度时会对土壤性质和土壤生物多样性造成危害。一般认为,塑料可根据其大小分为尺寸小于5 mm的微塑料、介于5~25 mm的中等塑料和大于25 mm的大塑料,还可以根据其形态分为球状、薄膜状、纤维状和碎片状[5]。常见的分布于土壤中的塑料种类有聚苯乙烯(PS)、聚乙烯(PE)、聚丙烯(PP)、高密度聚乙烯(HDPE)、低密度聚乙烯(LDPE)和聚乳酸(PLA)等。塑料在人类生产生活当中分布广、用途多,性质稳定且难以被分解,分布在土壤中的微塑料改变了土壤理化性质和物质循环[6],纳米微塑料能够被植物吸收[7-9],威胁人畜生命健康,也可直接被无脊椎动物摄食,部分难以排出体外,逐级积累在更高等的动物体内[10]。人体粪便中检测到多达9种微塑料[11],长期暴露在高浓度微塑料环境下的塑料行业工人,更容易患多种癌症[12]。目前微塑料的生态效应和对人类身体健康产生的危害仍有待深入研究[13]。
土壤植物系统包括土壤和植物(或作物)两个部分,如农田、林地、草原、湿地等,不仅是联系城乡生态系统的纽带,也是沟通植物和动物的桥梁,具有重要生态功能。本文以土壤-植物系统中的微塑料为对象,综述了农田等不同土壤中微塑料的来源、分布及迁移,分析其对土壤环境,包括物理性质、土壤微生物、土壤动物的影响,以及对植物的生态效应,以期为了解微塑料对土壤-植物系统的生态效应提供参考。
1 土壤中微塑料的来源、分布及迁移土壤中的微塑料来源于市政污泥(包括化妆品、衣物及工业生产过程产生的塑料沉积)的土地利用、农用地膜和塑料垃圾的残留分解、大气微塑料的沉降、地表径流和农用灌溉水的引入。由于污水处理厂提取污泥的一般处理步骤(如过滤、干燥、杀菌、堆肥等)不会消除微塑料,因而污泥堆肥后作为肥料施加到农田土中,成为土壤中微塑料的主要来源[14]。在欧洲,每年每百万居民会排放1 270~2 130 t微塑料到环境中[15]。同样,污水处理厂处理后的废水仍存在大量的微塑料,用其灌溉农作物成为土壤中微塑料的来源之一[16]。在中国,由于农用地膜的使用越来越广泛,其覆盖面积已达1 840万hm2,年使用量高达146.8万t(来自农业农村部2016年统计数据),使用过后的农膜残留并积累在土壤中形成塑料污染[17]。城市及工业塑料垃圾如农业工具、塑料包装材料和一些生活塑料垃圾经光照、高温及土壤磨损等作用,在环境中分裂或降解,或经土壤动物的消化后生成次生微塑料散布在土壤中。已有报道指出,不同类型不同粒径的微塑料可通过输移和干/湿沉降将微塑料从大气中运送到偏远地区的陆地和湖泊中,文献中有记载的最远距离高达95 km[18-19],也可通过降雨降雪等汇入地表径流将微塑料引入到土壤甚至地下水中[20]。
微塑料在土壤环境中经光氧化途径使塑料碎片化的过程尤为缓慢,所以普遍认为土壤是微塑料的储存库[21]。目前土壤微塑料的调查主要集中于农田、菜地、果园等农用地(表 1)。Ding等[22]对陕西省黄土高原、关中平原、秦巴山区9市的农用土壤进行了调查,全部样品中均发现微塑料,丰度高达1 430~3 410 ind·kg-1,其中黄土高原的土样微塑料丰度较高。Huang等[17]对我国19省份的农膜覆盖土壤进行了调查,发现微塑料含量随覆膜年限而升高。这意味着农业措施尤其是覆膜是微塑料的重要来源。Zhou等[23]发现杭州湾滨海平原覆膜农田土壤中微塑料丰度高于未覆膜土壤,但农膜并非唯一来源。来自德国[24]、智利[16]的调查则证实农业土壤中的微塑料污染与污水污泥的施用密切相关。微塑料丰度与土地利用类型密切相关,如在韩国骊州[25],路边土壤中微塑料的含量显著高于林地和居住用地,其原因主要是由于轮胎灰尘和道路涂料以及其他用于建筑油漆和交通安全设施的材料会在周围环境中产生微塑料残留物,而林地受人为活动影响较小,因而微塑料丰度较低。来自武汉郊区的调查则发现林地土壤中的微塑料含量高于菜地,而空地土壤中的含量最低[26]。在湿地[27]、庭园[10]、漫滩土[28]、工业土壤[29]中也均有微塑料检出。考虑到土壤微塑料的来源,微塑料很可能广泛分布于陆地生态系统。需要指出是,目前尚缺乏标准化的土壤微塑料分离方法,土壤微塑料污染状况尚需深入调查,目前已有的结果不能进行草率比较。此外,微塑料在植物尤其是农作物中的污染分布特征尚没有研究,未来需要关注。
微塑料的化学性质稳定且可以在环境中持久存在,在环境中的迁移方式主要有两种(图 1),一是通过自然条件,包括天气因素(如风力、潮汐、径流和降水)、地貌、重力和生物作用等;二是通过人类生产活动如工业生产、垃圾填埋等产生[40]。在土壤中的迁移方式可分为多种,可通过重力沉降和降水渗透进入到地下水系统[41],也可通过蚯蚓等无脊椎动物的活动,沿着土壤剖面向下运输[42]。当微塑料分解到纳米级就会被植物根系通过吸附作用转移到土壤上层,也会被无脊椎动物或昆虫等通过吞食作用吸收到体内后被鸡等动物捕食,沿食物链传播[10]。
微塑料对土壤生态系统的影响研究较少,原因可能是土壤是一个复杂的非均质系统,相较于海洋环境更加复杂多变,土壤中的微塑料更难以分离检测[43]。不同粒径和种类的微塑料对土壤-植物系统有一系列的直接影响,例如,改变土壤理化性质,促进土壤中微生物群落的分化演替,使土壤动物产生氧化应激反应,部分纳米级的微塑料甚至能被植物吸收产生毒性效应。
2.1 微塑料对土壤理化性质的影响微塑料在土壤中残留会导致土壤pH、电导率(EC)、有机质和养分的有效性改变[44]。土壤中添加HDPE使土壤pH降低[45-46],PLA使土壤pH升高和EC降低[46],而PS则没有显著影响[45]。有研究表明高浓度(28%,w/w)的微塑料会降低溶解性有机物的分解速率,提高土壤养分[47],但农田土中的草甘膦等农药成分与微塑料相互作用会导致土壤中溶解性有机碳和有机磷的损失,降低土壤养分[48-49]。生物可降解塑料如PLA可以降低土壤中铵态氮浓度,影响氮元素循环[50]。不同类型、不同浓度的微塑料对土壤物理性质的影响有所差异(表 2),其中粒径较大、目测可见的微塑料自身的吸附效应会影响土壤结构组成和容重[51-52]。平均直径 < 5 μm的超细聚酯纤维(0.3%,w/w)添加到土壤中有利于土壤团聚体的形成,增大土壤孔隙率,降低土壤的持水能力[53-54],加快水分蒸发[55]。平均直径18 μm的聚丙烯纤维(0.4%,w/w)和平均直径8 μm的聚酯纤维(0.4%,w/w)均能显著降低土壤水稳性团聚体,导致土壤贫瘠化[51]。土壤性质的改变会对微生物群落(由细菌、真菌、原生动物和其他生物)产生直接或间接的作用,进一步影响整个土壤-植物系统[56]。
微塑料影响土壤微生物群落结构和土壤酶活性(表 3)。LDPE能改变土壤微生物群落结构,导致土壤中细菌群落演替差异越来越大[57],PE薄膜使土壤结构更加松散,增大了微生物的附着面积,使微生物在塑料表面形成一层生物膜[58]。这层生物膜能提高微生物活性,使土壤中脲酶和过氧化氢酶等酶活性显著升高[59-60]。磷脂脂肪酸(Phospholipid fatty acids,PLFAs)是几乎所有活体细胞膜的主要成分,由1%(w/w)浓度的LDPE和PP处理后的土壤PLFAs增加,证实微塑料的添加对土壤微生物有促进作用[61]。微塑料中含碳量相对较高,会导致土壤碳氮比(C/N)增加,进而影响微生物的固定,尤其是那些较易降解的塑料[62]。土壤中与碳(β-葡萄糖苷酶和纤维二糖水解酶)、氮(亮氨酸氨基肽酶)、磷(碱性磷酸酶)循环[50, 63]相关的胞外酶活性的降低与土壤微生物生物量碳和脱氢酶活性的降低相一致,表明微塑料对土壤微生物有不利影响[64]。同时微塑料自身含有的有害物质会释放到土壤中,如塑料中所含的双酚A和邻苯二甲酸酯等释放到土壤中,对土壤微生物活性有抑制作用[65]。我们的研究首次发现,微塑料能够改变丛枝菌根真菌的群落结构和多样性,但是与微塑料的类型有关,可降解微塑料PLA的影响较HDPE更为显著[46]。
土壤动物具有重要生态功能,影响有机质分解、营养元素循环和能量流动[67],从而直接和间接影响植物生长。微塑料在被动物摄取后,在其体内存留会对器官和组织产生不利影响,也由于微塑料的摄入代替了部分食物,引起营养和能量短缺。表 4显示,微塑料对蚯蚓和线虫等动物具有一定毒性,多数情况下微塑料使生物量和繁殖率降低、死亡率升高。蚯蚓促进了微塑料在土壤中的运输[68],显著减轻了塑料残留对植物的危害[69],但高浓度(1%和2%,w/w)的PS对蚯蚓的生长有明显抑制作用,并增加蚯蚓的表面损伤[70]和死亡率[71]。轮胎颗粒显著降低土壤线蚓的存活率,对其繁殖率的抑制作用随浓度增加而加强,同时改变了其肠道和周围土壤中微生物的群落结构组成[72]。对于线虫而言,微塑料降低繁殖率,使幼虫数量减少,但是与微塑料种类和浓度密切相关[73-74]。
微塑料可直接影响植物,延缓种子萌发,抑制植物生长[77-78],并对植物产生生态毒性和遗传毒性[79]。植物细胞壁孔洞约5~50 nm,介于此粒径的微塑料更容易吸附在种子表皮或根系细胞壁孔洞,堵塞种子囊中的孔,且在生长后期,根毛上累积了微塑料[77],扰乱了种子或根系对水分、营养的正常吸收或运输,从而导致植物生长受抑[80]。微塑料尤其是纳米塑料一旦被可食用植物吸收,就可能沿着食物链在生物体和人体内积累,从而威胁人类健康。李连祯等[7]将荧光标记与激光共聚焦扫描电镜结合起来观察微塑料在植物体内的分布和运输,发现亚微米级PS微珠可以通过质外体运输穿过细胞间隙聚集在小麦根的木质部和皮层组织的细胞壁上。微珠进入中柱后,就可以随着蒸腾作用向植物的上部移动,通过茎叶通孔从根转移到茎和叶,最后通过质外体途径转移到叶脉脉管。微塑料不仅可以被植物吸收,也对植物生长和性状造成一定的影响(表 5)。植株生物量和根茎长度常被用来衡量毒性效应,微塑料的添加会降低小麦总生物量,抑制株高和根长[69, 81-82],但会增高拂子茅和黑麦草的根系生物量[83-84]。有研究发现PA(2.0%,w/w)能使葱鳞茎的含水量增加一倍,而PES(0.2%,w/w)、PET(2.0%,w/w)、PP(2.0%,w/w)会降低其含水量[85],除PP没有显著影响植物生物总量外,其他微塑料均有一定的促进作用。从表 5看出,目前的模拟试验有些微塑料暴露浓度偏高,未来需要参考田间调查数据,选择现实浓度进行研究。
最近有研究指出,当纳米塑料带不同电荷时,对拟南芥的生长抑制效果不同,带正电荷的微塑料稳定性较差,更容易被植物细胞的纤维素成分吸引,从而吸附到细胞壁表面造成堵塞[90]。微塑料的粒径也是重要影响因素,据荧光标记扫描电镜观察0.2 μm的PS可传输至小麦茎叶中,而2 μm的PS并未在此组织中观察到[91]。微米级PE塑料在10、50和100 mg·L-1时均显著抑制了蚕豆的生长,但纳米PE仅在100 mg·L-1时抑制了蚕豆的生长,且纳米级对蚕豆的生态毒性和遗传毒性较微米级要大[79]。当PE微塑料尺寸介于8.3±0.5 mm时并不影响农田土壤中绿豆、莴苣和水稻的生长[92]。在沙培条件下,粒径在0.55~0.8 mm、0.106~0.15 mm的HDPE对绿豆生长均没有显示出抑制作用,甚至在一定浓度时有刺激作用,而粒径0.023~0.038 mm时却对植株生长有一定抑制作用[93]。微塑料老化程度也是对植物造成不同影响的关键因素。对于初生微塑料而言,物理作用对植物根系破坏较大,而对于老化微塑料,表面粗糙程度增加,附着的污染物也相应增加,从而对植物根系造成直接毒性影响[94]。
3 微塑料对土壤-植物系统的间接效应微塑料也可以间接作用于土壤-植物系统,例如微塑料可以通过改变土壤理化性质、土壤微生物活性、土壤动物、土壤污染物等环境因子和生物因子而间接作用于植物。如表 2所示,微塑料能够改变土壤团聚体结构、容重和土壤持水性,这些性质的改变势必会影响植物生长。Lozano等[89]研究发现微塑料纤维降低了土壤容重,导致土壤大孔隙和通气量增加,有助于根系在土壤中的渗透,从而促进根系生长;而微塑料薄膜增加了地上部和根部的质量,可能是由于土壤容重的降低以及相关土壤性质的改善所致。随着微塑料薄膜浓度的增加,地上部和根系质量的减少可能是由于增加了水分运动的通道,增加了土壤水分蒸发率。微塑料纤维可以缓解干旱对植物生长带来的不利影响,改变植物群落结构和生产力[84]。在小麦生长过程中,LDPE(1%,w/w)对其产生了负面效应,一方面原因可能是因为微塑料的残留改变了土壤性质(土壤pH、EC和C/N)[69],影响植物对水分的吸收,另一方面可能是微塑料的存在导致根际挥发性有机物的改变(细菌产生的十二甲烷),这些挥发性产物具有植物生长诱导和生长抑制作用。
微塑料会影响土壤微生物活性,尤其是土壤酶活性(表 3),脲酶、磷酸酶等土壤酶活性的改变会影响养分有效性,间接影响植物养分吸收。有研究发现,土壤中添加PA增加了叶片氮含量、C/N降低,而PES则降低了叶片氮含量,使C/N升高[85]。添加LDPE和可降解微塑料对豆科植物中根瘤共生有一定的促进作用[87],这意味微塑料很可能会影响根瘤菌活性和固氮功能。土壤中添加PES(0.2%)使植物菌根侵染率增加了8倍,PP(2.0%)处理增加了1.4倍,而PET(2.0%)处理却降低了50%。根瘤菌、菌根真菌等可与植物共生,改善植物氮、磷等营养,微塑料对植物共生微生物的影响值得深入研究。
土壤动物如蚯蚓可以改善土壤结构、提高土壤肥力,促进植物生长,而某些线虫则可引起植物病害,对植物生长不利。Boots等[83]研究发现蚯蚓与微塑料共同作用,可能会改变土壤pH和土壤水稳性团聚体的粒径分布。微塑料对土壤动物的生存和繁殖不利(表 4),很可能会进一步影响其生态功能和植物生长,有关效应和机制均需进一步研究。
微塑料可以作为有机污染物和重金属的载体对土壤-植物系统产生间接毒性。影响微塑料对有机物和重金属的吸附因素有很多,例如塑料的老化程度[95],土壤pH、温度、盐度、阴阳离子浓度等[96]。在农业生产过程中使用的农药和抗生素可被吸附在微塑料的孔隙中,从而延长持久性[97-99],其吸附机理主要由微塑料本身的疏水性决定,吸附程度取决于比表面积和范德华力。有机化合物(如有机氯农药、多环芳烃、多氯联苯等)具有很高的辛醇/水分配系数(Kow)和疏水性,与微塑料的特性类似,两者更容易相互吸附[100]。根据目前研究,微塑料本身毒性并不是特别强(表 5),但与其他污染物共存时可能改变其在土壤中的移动性和生物效应,对植物和土壤微生物造成更严重的危害[45-46, 101]。土壤中的微塑料通过物理吸附和共沉降,能降低重金属的交换态、碳酸盐结合态和铁锰氧化物结合态,增加有机结合态,这样的作用会降低重金属在土壤中的生物有效性和迁移率[102],从而降低重金属对作物的毒性[103]。但我们的研究[104]发现,与土壤相比,HDPE微塑料对镉的吸附能力要低得多,土壤中添加HDPE会降低土壤对镉的吸附,而且被HDPE吸附的镉更容易解吸。进一步研究[45-46]发现,土壤中添加HDPE、PS、PLA等往往导致土壤中镉的生物有效性增加,进而影响植物生长和微生物群落结构。Abbasi等[105]发现PET颗粒可以作为载体将三种重金属(镉、铅、锌)迁移至小麦根际,并在此进行解吸,从而更有利于向植物体中转移。由此可知,重金属可被富集也可被解吸释放,导致微塑料与重金属的联合毒性大于单独处理的效果[45-46, 106]。
4 研究展望土壤微塑料种类多样、形态各异、性质多样,而土壤体系是一个复杂的体系,微塑料在土壤-植物系统中的效应仍有一系列问题待深入探究。未来需重点关注以下几个方面:
1)需进一步明确土壤-植物系统尤其是农业生态系统中微塑料的来源、分布和迁移途径及影响因素,分析微塑料是否能够被田间作物吸收和转运以及是否进入食物链,进一步评估微塑料对植物的毒性和健康风险。
2)由于土壤成分复杂,对土壤微塑料的分离和鉴定需提出更高的要求,未来需要建立准确高效的土壤微塑料分离、定性和定量表征方法,为深入研究土壤-植物系统中微塑料来源、污染程度和生态风险提供技术标准。
3)微塑料很可能会影响土壤养分、水分的有效性,进而影响植物生长发育,未来需要深入探明微塑料通过改变土壤性质和养分、水分循环等引起的植物间接毒性机制。
4)目前的研究多是在室内条件下的短期研究,微塑料暴露浓度偏高,而且大多使用初加工微塑料,而进入土壤中的微塑料则形态各异,老化程度也各有不同,不同的土壤环境中浓度也可能差异较大,未来应开展多尺度试验和长期试验,深入了解微塑料类型、形状、尺寸、剂量、老化程度等因素对微塑料生态效应的影响。
5)微塑料自身释放的化学物质(如增塑剂、阻燃剂、抗氧化剂和稳定剂等)以及通过吸附解吸作用释放的污染物对生态系统和人类健康存在潜在威胁,微塑料作为污染物载体的生态效应研究仍相对较少,需要对微塑料与污染物在土壤-植物系统中的复合生态效应进行深入探讨。
6)在探究微塑料对土壤-植物的生态效应时,应充分考虑各种因素之间的复合作用,如不同土壤性质对微塑料生态效应的影响、不同微塑料组合对植物个体和群落的影响、微塑料对植物与微生物共生效应的影响、环境胁迫条件下微塑料的生态效应,以全面评估微塑料对土壤-植物系统的潜在危害和生态风险。
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